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Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions Qi Wang University of Kentucky

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Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions Qi Wang University of Kentucky University of Kentucky UKnowledge Plant and Soil Sciences Faculty Publications Plant and Soil Sciences 3-9-2018 Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions Qi Wang University of Kentucky Jinge Liu University of Kentucky, [email protected] Hongyan Zhu University of Kentucky, [email protected] Right click to open a feedback form in a new tab to let us know how this document benefits oy u. Follow this and additional works at: https://uknowledge.uky.edu/pss_facpub Part of the Bacteria Commons, Genetics and Genomics Commons, and the Plant Sciences Commons Repository Citation Wang, Qi; Liu, Jinge; and Zhu, Hongyan, "Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume- Rhizobium Interactions" (2018). Plant and Soil Sciences Faculty Publications. 105. https://uknowledge.uky.edu/pss_facpub/105 This Review is brought to you for free and open access by the Plant and Soil Sciences at UKnowledge. It has been accepted for inclusion in Plant and Soil Sciences Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact [email protected]. Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions Notes/Citation Information Published in Frontiers in Plant Science, v. 9, article 313, p. 1-8. Copyright © 2018 Wang, Liu and Zhu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Digital Object Identifier (DOI) https://doi.org/10.3389/fpls.2018.00313 This review is available at UKnowledge: https://uknowledge.uky.edu/pss_facpub/105 fpls-09-00313 March 7, 2018 Time: 15:55 # 1 MINI REVIEW published: 09 March 2018 doi: 10.3389/fpls.2018.00313 Genetic and Molecular Mechanisms Underlying Symbiotic Specificity in Legume-Rhizobium Interactions Qi Wang†, Jinge Liu† and Hongyan Zhu* Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, United States Legumes are able to form a symbiotic relationship with nitrogen-fixing soil bacteria called rhizobia. The result of this symbiosis is to form nodules on the plant root, within which the bacteria can convert atmospheric nitrogen into ammonia that can be used by the plant. Establishment of a successful symbiosis requires the two symbiotic partners to be compatible with each other throughout the process of symbiotic development. However, incompatibility frequently occurs, such that a bacterial strain is unable to nodulate a particular host plant or forms nodules that are incapable of fixing nitrogen. Genetic and Edited by: molecular mechanisms that regulate symbiotic specificity are diverse, involving a wide Jeanne Marie Harris, range of host and bacterial genes/signals with various modes of action. In this review, University of Vermont, United States we will provide an update on our current knowledge of how the recognition specificity Reviewed by: Arijit Mukherjee, has evolved in the context of symbiosis signaling and plant immunity. University of Central Arkansas, Keywords: legume, nodulation, nitrogen fixation, rhizobial symbiosis, host specificity United States Dong Wang, University of Massachusetts Amherst, United States INTRODUCTION *Correspondence: Hongyan Zhu The legume-rhizobial symbiosis starts with a signal exchange between the host plant and its [email protected] microsymbiont (Oldroyd, 2013). Recognition of compatible bacteria by the host induces cortical †These authors have contributed cell divisions to form root nodule primordia, and simultaneously initiates an infection process to equally to this work. deliver the bacteria into the nodule cells. Infection of most legumes involves the development of plant-made infection threads that initiate in the root hair. The infection threads harboring dividing Specialty section: bacteria grow through the epidermal cell layer into the nodule cells, where the bacteria are released This article was submitted to and internalized in an endocytosis-like process. In nodule cells, individual bacteria are enclosed Plant Evolution and Development, by a membrane of plant origin, forming an organelle-like structure called the symbiosome, within a section of the journal which the bacteria further differentiate into nitrogen-fixing bacteroids (Jones et al., 2007; Oldroyd Frontiers in Plant Science et al., 2011). Received: 27 November 2017 Symbiotic nodule development involves synchronous differentiation of both nodule and Accepted: 23 February 2018 bacterial cells. Legume nodules can be grouped into two major types: indeterminate (e.g., 09 March 2018 Published: pea, clovers, and Medicago) and determinate (e.g., soybeans, common bean, and Lotus)(Nap Citation: and Bisseling, 1990; Hirsch, 1992). Indeterminate nodules originate from cell divisions in the Wang Q, Liu J and Zhu H (2018) inner cortex and possess a persistent apical meristem. Consequently, indeterminate nodules are Genetic and Molecular Mechanisms Underlying Symbiotic Specificity cylindrical in shape, with a developmental gradient from the apex to the base of the nodule, which in Legume-Rhizobium Interactions. can be divided into different nodule zones (Nap and Bisseling, 1990). In contrast, determinate Front. Plant Sci. 9:313. nodules result from cell divisions in the middle/outer cortex of the root, lack a persistent meristem, doi: 10.3389/fpls.2018.00313 and are spherical in shape. Cell divisions of a determinate nodule cease at early developmental Frontiers in Plant Science| www.frontiersin.org 1 March 2018| Volume 9| Article 313 fpls-09-00313 March 7, 2018 Time: 15:55 # 2 Wang et al. Specificity in Legume Symbiosis stages and the mature nodule develops through cell enlargement; NodD proteins from different rhizobia are adapted to as such, the infected cells develop more or less synchronously recognizing different flavonoids secreted by different legumes, to the nitrogen-fixing stage. In both nodule types, the and this recognition specificity defines an early checkpoint of symbiotic nodule cells undergo genome endoreduplication, the symbiosis (Peck et al., 2006). Despite the absence of direct leading to polyploidization and cell enlargement. Parallel to the evidence for physical interaction between the two molecules, nodule cell development is the differentiation of the nitrogen- flavonoids have been shown to be able to stimulate the binding fixing bacteroids. Depending on the host, but independent of NodD to nod gene promoters in Sinorhizobium meliloti (Peck of the nodule type, such bacterial differentiation can be et al., 2006). It is well documented that inter-strain exchange terminal or reversible. Terminal differentiation is featured by of nodD genes can alter the response of the recipient strain to genome endoreduplication, cell elongation, increased membrane a different set of flavonoid inducers and hence the host range permeability, and loss of reproductive ability, while in reversible (Horváth et al., 1987; Perret et al., 2000). For example, the differentiation the bacteroids retain cell size and DNA content transfer of nodD1 from the broad host range symbiont Rhizobium similar to free-living bacteria (Kereszt et al., 2011; Oldroyd sp. NGR234 to the restricted host range strain Rhizobium et al., 2011; Haag et al., 2013). Compared to free-living bacteria, leguminosarum biovar trifolii ANU843 enabled the recipient the bacteroids display dramatic changes in transcriptome, cell strain to nodulate the non-legume Parasponia, because the wide- surface structure and metabolic activities so that they become host-range NodD1 protein is capable of recognizing a broader better adapted to the intracellular environment and dedicated to spectrum of flavonoid inducers (Bender et al., 1988). nitrogen fixation (Mergaert et al., 2006; Prell and Poole, 2006; The evidence for the importance of flavonoids in determining Haag et al., 2013). host range primarily comes from bacterial genetics, and the Both legumes and rhizobial bacteria are phylogenetically plant genes involved are less studied. Since legume roots secrete diverse. No single rhizobial strains can form symbiosis with a complex mixture of flavonoid compounds, it is difficult to all legumes, and vice versa. Specificity occurs at both species pinpoint which flavonoids play a more critical role, and when and genotypic levels (Broughton et al., 2000; Perret et al., 2000; and where they are produced. Recent studies in soybeans and Wang et al., 2012). This can take place at early stages of the Medicago truncatula have highlighted key flavonoids required interaction so that the same bacterial strains can infect and for rhizobial infection (reviewed in Liu and Murray, 2016). nodulate one host plant but not another (Yang et al., 2010; Wang These so called “infection flavonoids” are strong inducers of nod et al., 2012; Tang et al., 2016; Fan et al., 2017). Incompatibility genes, secreted by roots, highly accumulated at the infection also frequently happens at later stages of nodule development sites, and show increased biosynthesis in response to infection such that nitrogen-fixing efficiency differs significantly between by compatible rhizobia. Although luteolin was the first flavonoid different plant-bacteria combinations (Wang et al., 2012,
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